A community perspective on the concept of marine holobionts: current status, challenges, and future directions Simon M. Dittami1, Enrique Arboleda2, Jean-Christophe Auguet3, Arite Bigalke4, Enora Briand5, Paco Cárdenas6, Ulisse Cardini7, Johan Decelle8, Aschwin H. Engelen9, Damien Eveillard10, Claire M.M. Gachon11, Sarah M. Griffiths12, Tilmann Harder13, Ehsan Kayal2, Elena Kazamia14, Francois¸ H. Lallier15, Mónica Medina16, Ezequiel M. Marzinelli17,18,19, Teresa Maria Morganti20, Laura Núñez Pons21, Soizic Prado22, José Pintado23, Mahasweta Saha24,25, Marc-André Selosse26,27, Derek Skillings28, Willem Stock29, Shinichi Sunagawa30, Eve Toulza31, Alexey Vorobev32, Catherine Leblanc1 and Fabrice Not15 1 Integrative Biology of Marine Models (LBI2M), Station Biologique de Roscoff, Sorbonne Université, CNRS, Roscoff, France 2 FR2424, Station Biologique de Roscoff, Sorbonne Université, CNRS, Roscoff, France 3 MARBEC, Université de Montpellier, CNRS, IFREMER, IRD, Montpellier, France 4 Institute for Inorganic and Analytical Chemistry, Bioorganic Analytics, Friedrich-Schiller-Universität Jena, Jena, Germany 5 Laboratoire Phycotoxines, Ifremer, Nantes, France 6 Pharmacognosy, Department of Medicinal Chemistry, Uppsala University, Uppsala, Sweden 7 Integrative Marine Ecology Dept, Stazione Zoologica Anton Dohrn, Napoli, Italy 8 Laboratoire de Physiologie Cellulaire et Végétale, Université Grenoble Alpes, CNRS, CEA, INRA, Grenoble, France 9 CCMAR, Universidade do Algarve, Faro, Portugal 10 Laboratoire des Sciences Numériques de Nantes (LS2N), Université de Nantes, CNRS, Nantes, France 11 Scottish Marine Institute, Scottish Association for Marine Science, Oban, United Kingdom 12 School of Science and the Environment, Manchester Metropolitan University, Manchester, United Kingdom 13 University of Bremen, Bremen, Germany 14 Institut de Biologie, ENS, Paris, France Submitted 6 October 2020 15 Adaptation and Diversity in the Marine Environment, Station Biologique de Roscoff, Sorbonne Université, Accepted 16 January 2021 CNRS, Roscoff, France Published 25 February 2021 16 Department of Biology, Pennsylvania State University, University Park, United States of America 17 Corresponding authors Ecology and Environment Research Centre, The University of Sydney, Sydney, Australia Simon M. Dittami, 18 Singapore Centre for Environmental Life Sciences Engineering, Nanyang Technological University, [email protected] Singapore, Singapore Catherine Leblanc, 19 Sydney Institute of Marine Science, Mosman, Australia [email protected] 20 Max Planck Institute for Marine Microbiology, Bremen, Germany 21 Academic editor Section Biology and Evolution of Marine Organisms, Stazione Zoologica Anton Dohrn, Napoli, Italy 22 Konstantinos Kormas Molecules of Communication and Adaptation of Microorganisms (UMR 7245), National Museum of Natural History, CNRS, Paris, France Additional Information and 23 Instituto de Investigaciones Marinas, CSIC, Vigo, Spain Declarations can be found on 24 Benthic Ecology, Helmholtz Center for Ocean Research, Kiel, Germany page 19 25 Marine Ecology and Biodiversity, Plymouth Marine Laboratory, Plymouth, United Kingdom DOI 10.7717/peerj.10911 26 National Museum of Natural History, Département Systématique et Evolution, Paris, France 27 Faculty of Biology, University of Gdansk, Gdansk, Poland Copyright 28 Philosophy Department, University of Pennsylvania, Philadelphia, United States of America 2021 Dittami et al. 29 Laboratory of Protistology & Aquatic Ecology, Department of Biology, Ghent University, Ghent, Belgium Distributed under 30 Dept. of Biology, Institute of Microbiology and Swiss Institute of Bioinformatics, ETH, Zürich, Switzerland Creative Commons CC-BY 4.0 31 IHPE, Univ. de Montpellier, CNRS, IFREMER, UPDV, Perpignan, France 32 CEA - Institut de Biologie Francois¸ Jacob, Genoscope, Evry, France OPEN ACCESS How to cite this article Dittami SM, Arboleda E, Auguet J-C, Bigalke A, Briand E, Cárdenas P, Cardini U, Decelle J, Engelen AH, Eveillard D, Gachon CMM, Griffiths SM, Harder T, Kayal E, Kazamia E, Lallier FH, Medina M, Marzinelli EM, Morganti TM, Núñez Pons L, Prado S, Pintado J, Saha M, Selosse M-A, Skillings D, Stock W, Sunagawa S, Toulza E, Vorobev A, Leblanc C, Not F. 2021. A community perspective on the concept of marine holobionts: current status, challenges, and future directions. PeerJ 9:e10911 http://doi.org/10.7717/peerj.10911 ABSTRACT Host-microbe interactions play crucial roles in marine ecosystems. However, we still have very little understanding of the mechanisms that govern these relationships, the evolutionary processes that shape them, and their ecological consequences. The holobiont concept is a renewed paradigm in biology that can help to describe and understand these complex systems. It posits that a host and its associated microbiota with which it interacts, form a holobiont, and have to be studied together as a coherent biological and functional unit to understand its biology, ecology, and evolution. Here we discuss critical concepts and opportunities in marine holobiont research and identify key challenges in the field. We highlight the potential economic, sociological, and environmental impacts of the holobiont concept in marine biological, evolutionary, and environmental sciences. Given the connectivity and the unexplored biodiversity specific to marine ecosystems, a deeper understanding of such complex systems requires further technological and conceptual advances, e.g., the development of controlled experimental model systems for holobionts from all major lineages and the modeling of (info)chemical-mediated interactions between organisms. Here we propose that one significant challenge is to bridge cross-disciplinary research on tractable model systems in order to address key ecological and evolutionary questions. This first step is crucial to decipher the main drivers of the dynamics and evolution of holobionts and to account for the holobiont concept in applied areas, such as the conservation, management, and exploitation of marine ecosystems and resources, where practical solutions to predict and mitigate the impact of human activities are more important than ever. Subjects Ecology, Marine Biology, Microbiology Keywords Evolution, Ecosystem services, Symbiosis, Host-microbiota interactions, Marine holobionts, Dysbiosis RATIONALE, INTENDED AUDIENCE, AND SURVEY METHODOLOGY The idea of considering organisms in connection with the complex microbial communities they are associated with is a concept rapidly gaining in importance in a wide field of life and environmental sciences. It goes along with an increasing awareness that many organisms depend on complex interactions with their symbiotic microbiota for different aspects of their life, even though the extent of dependencies may vary strongly (Hammer, Sanders & Fierer, 2019). The host and its associated microbiota are considered a single ecological unit, the holobiont. This implies a real paradigm shift. Marine environments harbor most of the diversity of life in terms of the number of lineages that coexist, and the constant presence of surrounding water as a potential carrier of metabolites but also microbes facilitates tight interactions between these lineages, making a ``holistic'' view of these environments and the organisms that inhabit them particularly important. Dittami et al. (2021), PeerJ, DOI 10.7717/peerj.10911 2/34 This paper is intended for both scientists seeking an overview of recent developments in marine holobiont research and as a reference for policymakers. We review the state of the art in the field research and identify key challenges, possible solutions, and opportunities in the field. Our work is based on the result of a foresight workshop hosted in March 2018, which brought together an interdisciplinary group of 31 scientists. These scientists were selected for their complementary expertise in philosophy, evolution, computer sciences, marine biology, ecology, chemistry, microscopy, and microbiology, as well as for their work with a wide range of different model systems from phytoplankton, via macroalgae, corals, and sponges, to bacterial communities of hydrothermal vents. After a three-day brainstorming session, the resulting ideas and discussions were divided into different topics, and groups of two or more scientists were appointed to draft each section, each based on their expertise in the field, their knowledge of the literature, and literature searches. The assembled paper was then corrected and completed by the entire consortium. MARINE HOLOBIONTS FROM THEIR ORIGINS TO THE PRESENT The history of the holobiont concept Holism is a philosophical notion first proposed by Aristotle in the 4th century BC. It states that systems should be studied in their entirety, with a focus on the interconnections between their various components rather than on the individual parts (Met. Z.17, 1041b11–33). Such systems have emergent properties that result from the behavior of a system that is ``larger than the sum of its parts''. However, a major shift away from holism occurred during the Age of ``Enlightenment'' when the dominant thought summarized as ``dissection science'' was to focus on the smallest component of a system as a means of understanding it. The idea of holism started to regain popularity in biology when the endosymbiosis theory was first proposed by Mereschkowski (1905) and further developed by Wallin (1925). Still accepted today, this theory posits a single origin for eukaryotic cells through the symbiotic